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Tooth microwear pattern variation in karst and non-karst peninsular Southeast Asian murine rodents

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Abstract

The dietary preferences of most rodents, especially in tropical countries, are poorly known. In the tropics, rodent diversity can be high and several species can coexist in the same habitats. In order to better document the dietary habits of Southeast Asian murid and diatomyid rodents, we examined microwear patterns in 21 species, with a particular focus on those living in karst habitats. Five variables of microwear scars (scratches and pits) were counted and measured on the dental facet of the first molar hypocone. We observed large variation and overlap in microwear patterns between and within genera, suggesting that feeding ecology is diverse (mostly generalist omnivorous species) within species and genus. For species living in agro-ecosystems, few differences were observed when we compared sympatric species within a genus, suggesting that niche partitioning is not achieved by feeding, neither in terms of diet composition nor in the way food is processed, or that food items are more homogeneous in terms of physical properties that affect microwear patterns. Differences between sympatric species were more pronounced in forest or karst contexts, suggesting that specialisation and niche differentiation have persisted in more preserved environments. Finally, differences were also observed in urban ecosystems suggesting that the communities of rodents evolved niche partitioning in these human-modified habitats. Our results also revealed differences in microwear patterns between karst and non-karst rodents, with all karst species showing a trend towards increasing numbers of small scratches and small pits. This suggested that the karst environment may influence the dietary habits of rodents, either in terms of the composition of the diet or by altering the general characteristics of the food.

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Data Availability

All data and R scripts for this study are available in supplementary materials.

References

  • Alhajeri BH, Steppan SJ (2018) Disparity and evolutionary rate do not explain diversity patterns in muroid rodents (Rodentia: Muroidea). Evol Biol 45:324–344

    Article  Google Scholar 

  • Balakirev AE, Abramov AV, Tikhonov AN, Rozhnov VV (2012) Molecular phylogeny of the Dacnomys division (Rodentia, Muridae): the taxonomic positions of Saxtilomys and Leopoldamys. Dokl Biol Sci 445:251–254

    Article  CAS  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc 57:289–300

    Google Scholar 

  • Beynen PV, Townsend K (2005) A disturbance index for karst environments. Environ Manage 36:101–116

    Article  PubMed  Google Scholar 

  • Caporale SS, Ungar PS (2016) Rodent incisor microwear as a proxy for ecological reconstruction. Palaeogeogr Palaeoclimatol Palaeoecol 446:225–233

    Article  Google Scholar 

  • Chaisiri K, Chaeychomsri W, Siruntawineti J, Herbreteau V, Morand S (2010) Gastrointestinal helminth fauna in rodents from Loei province, Thailand. Srinakharinwirot Sci J 26:111–126

    Google Scholar 

  • Christensen HB (2014) Similar associations of tooth microwear and morphology indicate similar diet across marsupial and placental mammals. PloS One 9:e102789. https://doi.org/10.1371/journal.pone.0102789

  • Clements R, Sodhi NS, Schilthuizen M, NG, PK, (2006) Limestone karsts of Southeast Asia: Imperiled Arks of Biodiversity. Bioscience 56:733–752

    Article  Google Scholar 

  • Delang CO (2005) The political ecology of deforestation in Thailand. Geography 90:25–237

    Article  Google Scholar 

  • Denis C, Taylor PJ, Aplin KP (2017) Family Muridae. In: Handbook of the Mammals of the World: vol.7: rodents II. Lynx Edicions, Barcelona, pp 536−863

  • DeSantis LR, Scott JR, Schubert BW, Donohue SL, McCray BM, Stolk CA, Winburn AA, Greshko MA, O'Hara MC (2013) Direct comparisons of 2D and 3D dental microwear proxies in extant herbivorous and carnivorous mammals. PloS One. https://doi.org/10.1371/journal.pone.0071428

  • Firmat C, Gomes-Rodrigues H, Renaud S, Claude J, Hutterer R, Garcia-Talavera F, Michaux J (2010) Mandible morphology, dental microwear, and diet of the extinct giant rats Canariomys (Rodentia: Muridae) of the Canary island (Spain). Biol J Lin Soc 101:28–40

    Article  Google Scholar 

  • Francis CM (2019) Field guide to the mammals of South-East Asia, 2nd edn. Bloomsburry Publishing, London

    Google Scholar 

  • Ge D, Feijo A, Abramov AV, Wen Z, Liu Z, Cheng J, Xia L, Lu L, Yang Q (2021) Molecular phylogeny and morphological diversity of the Niviventer fulvescens species complex with emphasis on species in China. Zool J Linn Soc 191:528–547

    Article  Google Scholar 

  • Gillieson D (2005) Karst in Southeast Asia. In: the Physical Geography of Southeast Asia. Oxford University Press Inc. New York, pp 157−176

  • Ginot S, Claude J, Hautier L (2018a) One skull to rule them all? descriptive and comparative anatomy of the masticatory apparatus in five mouse species. J Morphol 279:1234–1255

    Article  PubMed  Google Scholar 

  • Ginot S, Herrel A, Claude J, Hautier L (2018b) Skull size and biomechanics are good estimators of in vivo bite force in murid rodents. Anat Rec 301:256–266

    Article  Google Scholar 

  • Gomes Rodrigues H, Merceron G, Viriot L (2009) Dental microwear patterns of extant and extinct Muridae (Rodentia, Mammalia): ecological implications. Naturwissenschaften 96:537–542

    Article  CAS  Google Scholar 

  • Gusovsky VV, Sinitsa MV (2021) Dietary preferences and autecology of a basal holarctic ground squirrel Spermophilinus (Rodentia: Sciuridae: Xerinae), inferred from dental microwear analysis. Hist Biol 33:54–61

    Article  Google Scholar 

  • Hardin G (1960) The competitive exclusion principle. Science 131(3409):1292–1297

    Article  CAS  PubMed  Google Scholar 

  • Hautier L, Bover P, Alcover JA, Michaux J (2009) Mandible morphometrics, dental microwear pattern, and paleobiology of the extinct balearic dormouse Hypnomys morpheus. Acta Paleontologica Polonica 54:181–194

    Article  Google Scholar 

  • Htwe NM, Singleton GR (2014) Is quantity or quality of food influencing the reproduction of rice-field rats in the Philippines. Wildl Res 41:56–63

    Article  Google Scholar 

  • Lacher TE, Young RP, Kennerley RJ, Turvey ST, Roach NS, McCay SD (2017) Conserving the biodiversity of the largest order of mammals: priorities and actions for the Rodentia. In: Handbook of the Mammals of the World: vol.7: rodents II. Lynx Edicions, Barcelona, pp 13−20

  • Langham L (1983) Distribution and ecology of small mammals in three rain forest localities of peninsula Malaysia with particular references to Kedah Peak. Biotropic 15:199–206

    Article  Google Scholar 

  • Latinne A, Galan M, Waengsothorn S, Rojanadilok P, Eiamampai K, Sribuarod K, Michaux JR (2014) Diet analysis of Leopoldamys neilli, a cave-dwelling rodent in Southeast Asia, using next-generation sequencing from feces. J Cave Karst Stud 76:139–145

    Article  Google Scholar 

  • Latinne A, Chaval Y, Waengsothorn S, Rojanadilok P, Eiamampai K, Sriburod K, Herbreteau V, Morand S, Michaux JR (2013a) Is Leopoldamys neilli (Rodentia, Muridae) a synonym of Leopoldamys herberti? A reply to Balakirev et al. (2013). Zootaxa 3731: 589–598.

  • Latinne A, Waengsothorn S, Rojanadilok P, Eiamampai K, Sriburod K, MichauxI JR (2013b) Diversity and endemism of murinae rodents in Thai limestone karsts. Syst. Biodivers. 11:323–344

  • Lekagul B, McNeely JA (1988) Mammals of Thailand, 2nd edn. Darnsutha Press, Bangkok

    Google Scholar 

  • Magioli M, Moreira MZ, Fonseca RC, Ribeiro MC, Rodrigues MG, Ferraz KM (2019) Human-modified landscapes alter mammal resource and habitat use and trophic structure. PNAS. https://doi.org/10.1073/pnas.1904384116

    Article  PubMed  PubMed Central  Google Scholar 

  • Martin SA, Alhajeri BH, Steppan SJ (2016) Dietary adaptations in the teeth of murine rodents (Muridae): a test of biomechanical predictions. Biol J Lin Soc 119:766–784

    Article  Google Scholar 

  • Martinez Q, Lebrun R, Achmadi AS, Esselstyn JA, Evans AR, Heaney LR, Miguez RP, Rowe KC, Fabre PH (2018) Convergent evolution of an extreme dietary specialisation, the olfactory system of worm-eating rodents. Sci Rep. https://doi.org/10.1038/s41598-018-35827-0

    Article  PubMed  PubMed Central  Google Scholar 

  • Morand S, Bordes F, Blasdell K, Pilosof S, Cornu JF, Chaisiri K, Chaval Y, Cosson JF, Claude J, Feyfant T, Herbreteau V, Dupuy S, Tran A (2015) Assessing the distribution of disease-bearing rodents in human-modified tropical landscapes. J Appl Ecol 52:784–794

    Article  Google Scholar 

  • Musser GG, Lund DP, Son NT (2006) Description of a new genus and species of rodent (Murinae, Muridae, Rodentia) from the tower karst region of Northeastern Vietnam. Am Mus Novit 3517:1–41

    Article  Google Scholar 

  • Musser GG, Smith AL, Robinson MF, Lunde DP (2005) Description of a new genus and species of rodent (Murinae, Muridae, Rodentia) from the Khammoun limestone national biodiversity conservation area in Lao PDR. Amer Mus Novit. https://doi.org/10.1206/0003-0082(2005)497[0001:DOANGA]2.0.CO;2

  • Nelson S, Badgley C, Zakem E (2005) Microwear in modern squirrels in relation to diet. Paleontol Electron 8:1–15

    Google Scholar 

  • Nguyen DX, Nguyen NX, Nguyen DD, Dinh TH, Le DT, Dinh DH (2014) Distribution and habitat of the Laotian rock rat Laonastes aenigmamus Jenkins, Kilpatrick, Robinson & Timmins, 2005 (Rodentia: Diatomyidae) in Vietnam. Biodivers Data J. https://doi.org/10.3897/BDJ.2.e4188

    Article  PubMed  PubMed Central  Google Scholar 

  • Nguyen NX, Nguyen DX, Ngo TX, Nguyen DD (2015) New data on recently described rodent species paulina’s limestone rat Saxatilomys paulinae Musser, Smith, Robinson & Lunde, 2005 (Mammalia: Rodentia). Biodivers Data J. https://doi.org/10.3897/BDJ.3.e4961

    Article  PubMed  PubMed Central  Google Scholar 

  • Oliver A, Hernandez-Ballarin V, Lopez-Guerrero P, Garcia-Paredes I, Alvarez-Sierra MA, Cano AR, Yelo BA, Alcalde GM, Pelaez-Campomanes P (2014) Dental microwear analysis in Gliridae (Rodentia): methodological issues and paleodiet inferences based on Armantomys from the Madrid Basin (Spain). J Iber Geol 40:157–166

    Article  Google Scholar 

  • Pagès M, Bazin E, Galan M, Chaval Y, Claude J, Herbreteau V, Michaux J, Piry S, Morand S, Cosson JF (2013) Cytonuclear discordance among Southeast Asian black rats (Rattus rattus complex) Mol Ecol 22(4):1019–1034. https://doi.org/10.1111/mec.12149

  • Pagès M, Chaval Y, Herbreteau V, Waengsothorn S, Cosson JF, Hugot JP, Morand S, Michaux J (2010) Revisiting the taxonomy of the Rattini tribe: a phylogeny-based delimitation of species boundaries. Evol Biol. https://doi.org/10.1186/1471-2148-10-184

    Article  Google Scholar 

  • R Core Team (2023) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Roberts N (2015) The cultural and natural heritage of caves in the Lao PDR: prospects and challenges related to their use, management and conservation. J Lao Stud 1:113−139

  • Rowe KC, Aplin KP, Baverstock PR, Moritz C (2011) Recent and rapid speciation with limited morphological disparity in the genus Rattus. Syst Biol 60:188–203

    Article  PubMed  Google Scholar 

  • Samuels JX (2009) Cranial morphology and dietary habits of rodents. Zool J Linn Soc 158:864–888

    Article  Google Scholar 

  • Shirako T, Ishizawa Y, Ajioka Y, Aichi M, Ueno K, Hoa DT, Hai BT, Thanh TV, Yamada M, Minami M (2015) Identification of Muridae species and their food resources using DNA barcoding in Cat Tien National Park. Vietnam Mamm Study 40:217–229

    Article  Google Scholar 

  • Steppan SJ, Schenk JJ (2017) Muroid rodent phylogenetics: 900-species tree reveals increasing diversification rates. PLoS One. https://doi.org/10.1371/journal.pone.0183070

    Article  PubMed  PubMed Central  Google Scholar 

  • Townsend K, Croft DA (2008) Enamel microwear in caviomorph rodents. J Mammal 89:730–743

    Article  Google Scholar 

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Acknowledgements

We thank the Institute of Evolutionary Science of Montpellier, the University of Montpellier, the National Science Museum of Thailand, the Chulalongkorn University Museum of Natural History and the Smithsonian National Museum of Natural History (Washington D.C.) for granting us access to the specimens. We are grateful to Sylvie Agret, Laurant Marivaux, Helder Gomes Rodrigues, Celine Robinet and Anne-lise Charruault for their help, discussion and techniques training. We thank all collaborators of the CERoPath project for their contributions to the rodent field trapping. We thank Ivan Calandra and an anonymous referee for their constructive remarks regarding an earlier version of the manuscript.

Funding

This research was funded by the Ministry of Higher Education, Science, Research and Innovation (Thailand) and the 90th Anniversary of Chulalongkorn University Fund (Ratchadaphiseksomphot Endowment Fund).

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Authors and Affiliations

  1. Ph.D. Program in Zoology, Department of Biology, Faculty of Science, Chulalongkorn University, Bangkok, 10330, Thailand

    Sirikorn Sripho

  2. Department of Biology, Faculty of Science, Chulalongkorn University, Bangkok, 10330, Thailand

    Thongchai Ngamprasertwong & Julien Claude

  3. Wildlife Conservation Society, Melanesia Program, Suva, Fiji

    Alice Latinne

  4. IRL HealthDEEP CNRS - Kasetsart University - Mahidol University, Faculty of Veterinary Technology, Kasetsart University, Bangkok, 10900, Thailand

    Serge Morand

  5. Institut Des Science de I’Evolution de Montpellier, Universite Montpellier, CNRS, IRD, Cc 064, Place Eugene Bataillon, 34095, Montpellier Cedex 5, France

    Julien Claude

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Contributions

Specimen captures: Sirikorn Sripho, Thongchai Ngamprasertwong, Serge Morand, Julien Claude and Alice Latinne; image analyses: Sirikorn Sripho; statistical analyses: Julien Claude and Sirikorn Sripho; text writing: Sirikorn Sripho and Julien Claude; text correction: Julien Claude, Serge Morand, Alice Latinne, Thongchai Ngamprasertwong and Sirikorn Sripho.

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Correspondence to Thongchai Ngamprasertwong.

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Sripho, S., Ngamprasertwong, T., Latinne, A. et al. Tooth microwear pattern variation in karst and non-karst peninsular Southeast Asian murine rodents. Mamm Res 69, 115–130 (2024). https://doi.org/10.1007/s13364-023-00723-0

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